The DOI matches its Crossref record; 4 of the 4 references it cites were found in a registry or an index.
The evolution of C4photosynthesis
Abstract
Summary: C 4 photosynthesis is a series of anatomical and biochemical modifications that concentrate CO 2 around the carboxylating enzyme Rubisco, thereby increasing photosynthetic efficiency in conditions promoting high rates of photorespiration. The C 4 pathway independently evolved over 45 times in 19 families of angiosperms, and thus represents one of the most convergent of evolutionary phenomena. Most origins of C 4 photosynthesis occurred in the dicots, with at least 30 lineages. C 4 photosynthesis first arose in grasses, probably during the Oligocene epoch (24–35 million yr ago). The earliest C 4 dicots are likely members of the Chenopodiaceae dating back 15–21 million yr; however, most C 4 dicot lineages are estimated to have appeared relatively recently, perhaps less than 5 million yr ago. C 4 photosynthesis in the dicots originated in arid regions of low latitude, implicating combined effects of heat, drought and/or salinity as important conditions promoting C 4 evolution. Low atmospheric CO 2 is a significant contributing factor, because it is required for high rates of photorespiration. Consistently, the appearance of C 4 plants in the evolutionary record coincides with periods of increasing global aridification and declining atmospheric CO 2. Gene duplication followed by neo‐ and nonfunctionalization are the leading mechanisms for creating C 4 genomes, with selection for carbon conservation traits under conditions promoting high photorespiration being the ultimate factor behind the origin of C 4 photosynthesis. ContentsSummary341I.Introduction342II.What is C 4 photosynthesis?343III.Why did C 4 photosynthesis evolve?347IV.Evolutionary lineages of C 4 photosynthesis348V.Where did C 4 photosynthesis evolve?350VI.How did C 4 photosynthesis evolve?352VII.Molecular evolution of C 4 photosynthesis361VIII.When did C 4 photosynthesis evolve362IX.The rise of C 4 photosynthesis in relation to climate and CO 2363X.Final thoughts: the future evolution of C 4 photosynthesis365Acknowledgements365References365
Overview
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Citations
Cites
The Evolutionary Fate and Consequences of Duplicate Genes
Lynch, M., & Conery, J. S. (2000) · Science · doi:10.1126/science.290.5494.1151 · Cited by 4,988
Atmospheric carbon dioxide concentrations over the past 60 million years
Pearson, P. N., & Palmer, M. R. (2000) · Nature · doi:10.1038/35021000 · Cited by 1,771
GEOCARB III: A revised model of atmospheric CO2 over Phanerozoic time
Berner, R. A. (2001) · American Journal of Science · doi:10.2475/ajs.301.2.182 · Cited by 1,323
Transcriptional regulators and the evolution of plant form
Doebley, J., & Lukens, L. (1998) · The Plant Cell · doi:10.1105/tpc.10.7.1075 · Cited by 421
Cited by
Improving photosynthetic efficiency for greater yield.
Zhu, X.-G., Long, S. P., & Ort, D. R. (2010) · Annual Review of Plant Biology · doi:10.1146/annurev-arplant-042809-112206 · Cited by 1,902
Can improvement in photosynthesis increase crop yields?
LONG, S. P., ZHU, X., NAIDU, S. L., & ORT, D. R. (2006) · Plant, Cell & Environment · doi:10.1111/j.1365-3040.2005.01493.x · Cited by 1,586
What Limits Trees in C4 Grasslands and Savannas?
Bond, W. J. (2008) · Annual Review of Ecology, Evolution, and Systematics · doi:10.1146/annurev.ecolsys.39.110707.173411 · Cited by 909
Photorespiration: players, partners and origin
Bauwe, H., Hagemann, M., & Fernie, A. R. (2010) · Trends in Plant Science · doi:10.1016/j.tplants.2010.03.006 · Cited by 652
The C4 plant lineages of planet Earth
Sage, R. F., Christin, P.-A., & Edwards, E. J. (2011) · Journal of Experimental Botany · doi:10.1093/jxb/err048 · Cited by 632
Self-citation
Metadata
- Authors
- Sage, R. F.
- Venue
- New Phytologist
- Publisher
- Wiley
- Published
- 2003-12-23
- Volume
- 161
- Issue
- 2
- Pages
- 341-370
- ISSN
- 0028-646X (ISSN-L)
- 1469-8137
- OpenAlex
- W2097616658
- Cited by
- 1,349
- References
- 4
- FWCI
- 19.32
- Type
- journal article
- Language
- en
- Open access
- closed
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
How to cite
Cite CoChat for the checks on this page, and the paper for its own findings.
- This page
- CoChat. (2026). Citation check: The evolution of C4photosynthesis. https://app.cochat.ai/papers/10.1111/j.1469-8137.2004.00974.x
- The paper
- Sage, R. F. (2004). The evolution of C4photosynthesis. New Phytologist. https://doi.org/10.1111/j.1469-8137.2004.00974.x
Data sources
Bibliographic data: Semantic Scholar, OpenAlex, Crossref.
Contains information from the Semantic Scholar Academic Graph Datasets, made available under the ODC Attribution License (ODC-BY 1.0).
Semantic Scholar’s data is described in: Kinney, R., et al. (2023). The Semantic Scholar Open Data Platform. arXiv:2301.10140.
